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Updates in Paracoccidioides Biology and Genetic Advances in Fungus Manipulation Journal of Fungi Review Updates in Paracoccidioides Biology and Genetic Advances in Fungus Manipulation Alison Felipe Alencar Chaves 1 , Marina Valente Navarro 1, Yasmin Nascimento de Barros 2, Rafael Souza Silva 1 , Patricia Xander 2 and Wagner Luiz Batista 1,2,* 1 Department of Microbiology, Immunology and Parasitology, Federal University of São Paulo, São Paulo 04023-062, Brazil; [email protected] (A.F.A.C.); [email protected] (M.V.N.); [email protected] (R.S.S.) 2 Department of Pharmaceutical Sciences, Federal University of São Paulo, Diadema 09913-030, Brazil; [email protected] (Y.N.d.B.); [email protected] (P.X.) * Correspondence: [email protected]; Tel.: +55-11-3319-3594; Fax: +55-11-3319-3300 Abstract: The dimorphic fungi of the Paracoccidioides genus are the causative agents of paracoccid- ioidomycosis (PCM). This disease is endemic in Latin America and primarily affects workers in rural areas. PCM is considered a neglected disease, despite being a disabling disease that has a notable impact on the public health system. Paracoccidioides spp. are thermally dimorphic fungi that present infective mycelia at 25 ◦C and differentiate into pathogenic yeast forms at 37 ◦C. This transition involves a series of morphological, structural, and metabolic changes which are essential for their survival inside hosts. As a pathogen, the fungus is subjected to several varieties of stress conditions, including the host immune response, which involves the production of reactive nitrogen and oxygen species, thermal stress due to temperature changes during the transition, pH alterations within phagolysosomes, and hypoxia inside granulomas. Over the years, studies focusing on under- Citation: Chaves, A.F.A.; Navarro, standing the establishment and development of PCM have been conducted with several limitations M.V.; de Barros, Y.N.; Silva, R.S.; Xander, P.; Batista, W.L. Updates in due to the low effectiveness of strategies for the genetic manipulation of Paracoccidioides spp. This Paracoccidioides Biology and Genetic review describes the most relevant biological features of Paracoccidioides spp., including aspects of Advances in Fungus Manipulation. J. the phylogeny, ecology, stress response, infection, and evasion mechanisms of the fungus. We also Fungi 2021, 7, 116. https://doi.org/ discuss the genetic aspects and difficulties of fungal manipulation, and, finally, describe the advances 10.3390/jof7020116 in molecular biology that may be employed in molecular research on this fungus in the future. Academic Editors: Carlos Keywords: neglected diseases; Paracoccidioides; mycosis; dimorphisms; paracoccidioidomycosis Pelleschi Taborda and Joshua Daniel Nosanchuk Received: 30 November 2020 Accepted: 2 February 2021 1. Introduction Published: 4 February 2021 1.1. Paracoccidioides and Paracoccidioidomycosis Paracoccidioides Publisher’s Note: MDPI stays neutral spp. is the aetiologic agent of paracoccidioidomycosis (PCM), a sys- with regard to jurisdictional claims in temic mycosis that mainly affects workers in rural areas and causes some degree of dis- published maps and institutional affil- ability for working-age people. In 1908, Adolpho Lutz described the causative agent of iations. PCM in the oral lesions and cervical lymph nodes of two patients. By that time, the disease and its agent received several names, until in 1930 Floriano Almeida finally proposed the name Paracoccidioides brasiliensis [1]. More recently, genomics analyses have identified the existence of cryptic species within the Paracoccidioides genus and new species have been proposed [2,3]. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. The disease is widely distributed in Latin American countries, such as Brazil [4], Ar- This article is an open access article gentina [5], Uruguay [6], Paraguay [7], Peru [8], Ecuador [9], Colombia [10], Venezuela [11], distributed under the terms and and Mexico [12]. However, there are reports of imported cases in such countries as conditions of the Creative Commons Japan [13], the Netherlands [14], Germany [15], and Austria [16] (Figure1). Due to the Attribution (CC BY) license (https:// reduced lethality and restricted geographic distribution of the etiological agent of PCM, creativecommons.org/licenses/by/ public health agencies have largely neglected the disease. PCM is geographically limited to 4.0/). Latin American countries and the highest number of reported cases are concentrated in J. Fungi 2021, 7, 116. https://doi.org/10.3390/jof7020116 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, 116 2 of 28 J. Fungi 2021, 7, 116 2 of 28 to Latin American countries and the highest number of reported cases are concentrated in Brazil (80%). Although Brazil reports more cases than any other country (Figure 1), these Brazilnumbers (80%). are Althoughprobably Brazilunderestimated, reports more given cases that than until any February other country 2020 (FigurePCM was1), these not a numbersnotifiable are disease, probably although underestimated, there is currently given that a untilrecommendation February 2020 for PCM reporting was not cases a noti- as fiableproven disease, or probable although [17] there. It is isexpected currently that a recommendation with this change, for the reporting data regarding cases as ep provenidemi- orology probable will soon [17]. be It ismore expected accurate. that with this change, the data regarding epidemiology will soon be more accurate. Figure 1. Epidemiological distribution of PCM cases throughout the world. The Netherlands, Germany, Austria, and Japan have imported cases. Legends show the name of the country and the number of cases identified through the period Figure 1. Epidemiological distribution of PCM cases throughout the world. The Netherlands, Germany, Austria, and Japan mentionedhave imported in each cases. study. Legends show the name of the country and the number of cases identified through the period men- tioned in each study. 1.2. Paracoccidioidomycosis: Disease, Diagnosis and Treatment 1.2. Paracoccidioidomycosis:PCM is a granulomatous Disease, disease Diagnosis that usually and Treatment presents in two distinct forms: acute or subacutePCM is and a granulomatous chronic forms. disease The acute that usually or subacute presents form in is two responsible distinct forms: for 5–25% acute of or casessubacute and and is characterized chronic forms. by The rapid acute dissemination or subacute toform the is reticuloendothelial responsible for 5–25% system. of cases In theand chronic is characterized form (74–96% by rapid of cases), dissemination the disease to progresses the reticuloendothelial slowly and may system. take months In the tochronic years toform become (74–96% apparent, of cases), and the pulmonary disease progresses manifestations slowly are and present may take in more months than to 90%years of to cases become [17,18 apparent,]. In addition, and pulmonary the chronic manifestations form can manifest are pr asesent unifocal in more or multifocal. than 90% Inof thecases unifocal [17,18] form. In addition, (25% of the cases), chronic the lungsform can and, manifest rarely, otheras unifocal sites are or multifocal. the only organs In the involvedunifocal form [19]. In(25% the of multifocal cases), the form, lungs along and, therarely, lungs, other the sites main are sites the involvedonly organs are involved the oral mucosa,[19]. In the skin, multifocal lymph nodes, form, and along adrenal the lung glandss, the and, main to asites lesser involved extent, are the the central oral nervousmucosa, system,skin, lymph bones, nodes genitals,, and andadrenal blood glands vessels. and, The to residuala lesser extent, form, observedthe central less nervous frequently, system, is expressedbones, genitals, by sequelae and blood left after vessels. treatment The [residual17]. form, observed less frequently, is ex- pressedThe clinicalby sequelae manifestations left after treatment of PCM can [17] be. related both to characteristics inherent to the pathogenThe andclinical to the manifestations host’s immune of responsePCM can profile.be related The both analysis to characteristics of the adaptive inherent immune to responsethe pathogen in different and to the clinical host’s spectra immune of PCMresponse has profile. contributed The analysis to a better of the understanding adaptive im- ofmune the diseaseresponse evolution. in different The clinical presence spectra of theof PCM T helper has contributed 2 (Th2)/Th9 to profilea better withunderstand- a high β productioning of the disease of cytokines evolution. IL-4, IL-5,The presence IL-9, IL-10, of TGF-the T helper, IL-27; 2 the(Th2)/Th9 polyclonal profile activation with a ofhigh B cells; the production of large amounts of specific IgG4, IgA, and IgE; and a low production of IFN-γ and TNF-α is related to the acute form of PCM with the fungus spreading to J. Fungi 2021, 7, 116 3 of 28 different organs and systems [20,21]. On the other hand, the prevalence of Th17 and Th22 with the production of the cytokines IFN-γ, TNF-α, and IL-2; varying amounts of IL-10 and IL-4; and the presence of high levels of specific IgG1 antibodies are immunological characteristics of the chronic form [20,21]. Asymptomatic and mild chronic forms have a Th1 profile, while the severe chronic form may have a predominance of Th2 response [21]. Interestingly, mice infected with different P. brasiliensis genotypes showed differences in their immune response profile, suggesting that factors of the pathogen may also contribute
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